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Scrutinizing the immune defence inventory of Camponotus floridanus applying total transcriptome sequencing.

Gupta SK, Kupper M, Ratzka C, Feldhaar H, Vilcinskas A, Gross R, Dandekar T, Förster F - BMC Genomics (2015)

Bottom Line: Based on homology analysis with key components of major immune pathways of insects, the C. floridanus immune-related genes were compared to those of Drosophila melanogaster, Apis mellifera, and other hymenoptera.The comparison of the immune system of C. floridanus with that of other insects revealed the presence of a broad immune repertoire.However, the relatively low number of PGN recognition proteins and AMPs, the identification of Camponotus specific putative immune genes, and stage specific differences in immune gene regulation reflects Camponotus specific evolution including adaptations to its lifestyle.

View Article: PubMed Central - PubMed

Affiliation: Department of Bioinformatics, Biocentre, University of Würzburg, Am Hubland, D-97074, Würzburg, Germany. shishir.bioinfo@gmail.com.

ABSTRACT

Background: Defence mechanisms of organisms are shaped by their lifestyle, environment and pathogen pressure. Carpenter ants are social insects which live in huge colonies comprising genetically closely related individuals in high densities within nests. This lifestyle potentially facilitates the rapid spread of pathogens between individuals. In concert with their innate immune system, social insects may apply external immune defences to manipulate the microbial community among individuals and within nests. Additionally, carpenter ants carry a mutualistic intracellular and obligate endosymbiotic bacterium, possibly maintained and regulated by the innate immune system. Thus, different selective forces could shape internal immune defences of Camponotus floridanus.

Results: The immune gene repertoire of C. floridanus was investigated by re-evaluating its genome sequence combined with a full transcriptome analysis of immune challenged and control animals using Illumina sequencing. The genome was re-annotated by mapping transcriptome reads and masking repeats. A total of 978 protein sequences were characterised further by annotating functional domains, leading to a change in their original annotation regarding function and domain composition in about 8% of all proteins. Based on homology analysis with key components of major immune pathways of insects, the C. floridanus immune-related genes were compared to those of Drosophila melanogaster, Apis mellifera, and other hymenoptera. This analysis revealed that overall the immune system of carpenter ants comprises many components found in these insects. In addition, several C. floridanus specific genes of yet unknown functions but which are strongly induced after immune challenge were discovered. In contrast to solitary insects like Drosophila or the hymenopteran Nasonia vitripennis, the number of genes encoding pattern recognition receptors specific for bacterial peptidoglycan (PGN) and a variety of known antimicrobial peptide (AMP) genes is lower in C. floridanus. The comparative analysis of gene expression post immune-challenge in different developmental stages of C. floridanus suggests a stronger induction of immune gene expression in larvae in comparison to adults.

Conclusions: The comparison of the immune system of C. floridanus with that of other insects revealed the presence of a broad immune repertoire. However, the relatively low number of PGN recognition proteins and AMPs, the identification of Camponotus specific putative immune genes, and stage specific differences in immune gene regulation reflects Camponotus specific evolution including adaptations to its lifestyle.

No MeSH data available.


Related in: MedlinePlus

The Toll signalling pathway of C. floridanus. All identified signalling components are mapped on the comprehensive immune network of D. melanogaster. The names of the factors correspond to the Drosophila designations. Connectivity among nodes is based either on positive attribute (blue arrow) or negative attribute (red arrow). Missing components are shown in grey colour. Nuclear translocation is shown by a green arrow. Factors significantly upregulated on the transcriptional level upon immune-challenge are shown by green boxes
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Fig5: The Toll signalling pathway of C. floridanus. All identified signalling components are mapped on the comprehensive immune network of D. melanogaster. The names of the factors correspond to the Drosophila designations. Connectivity among nodes is based either on positive attribute (blue arrow) or negative attribute (red arrow). Missing components are shown in grey colour. Nuclear translocation is shown by a green arrow. Factors significantly upregulated on the transcriptional level upon immune-challenge are shown by green boxes

Mentions: The Toll pathway of insects is mainly activated by fungal pathogens and Gram-positive bacteria. The Toll pathway not only regulates the antimicrobial response but is also required for proper haemocyte proliferation [4, 37]. Therefore, Toll activation leads to a coordinated immune response that comprises both cellular and humoral immunity [38]. The Toll signalling pathway was found to be highly conserved in terms of the presence of homologs in C. floridanus (Fig. 5). Recognition of Lys-type PGN characteristic for most Gram-positive bacteria or of fungal beta-1,3-glucans by specific PRRs leads to the activation of proteolytic cascades which finally activate the Toll-dependent signalling cascade. In C. floridanus three PRRs likely feeding into the Toll pathway are found: a PGRP-SA (Cflo_N_g8526t1) which according to sequence homology probably recognises Lys-type PGN, and two proteins annotated as beta-1,3-glucan binding proteins (Cflo_N_g15215t1 and Cflo_N_g5742t1) with high homologies to both GNBP1 and GNBP3 of D. melanogaster. GNBP1 is known to perceive Lys-type PGN, while GNBP3 recognises fungal cell wall components [39]. The homology data of the C. floridanus proteins do not allow a clear identification of the signal sensed by the two GNBPs. However, the previous expression data acquired post immune challenge of C. floridanus with Gram-negative or Gram-positive bacteria revealed a long-lasting up-regulation of the gene encoding one of the GNBPs (EFN66519.1; Cflo_N_g5742t1) only after infection with Gram-positive bacteria [17]. This suggests that this Camponotus protein may be able to recognise Lys-type PGN and thus may be a functional homolog of GNBP1 of D. melanogaster (Fig. 5). In addition, C. floridanus encodes a homolog of the protease Persephone which was previously shown to be involved in the detection of danger signals indicative for infection with Gram-positive bacteria and fungi [40]. In D. melanogaster the Toll pathway is triggered upon microbially induced proteolytic cleavage of the circulating cytokine-like ligand molecule Spätzle that binds to the Toll receptor, thus finally leading to the nuclear translocation of the NF-κB-like transcription factors Dorsal and DIF (Dorsal-related immunity factor). A single gene encoding Dorsal is present in C. floridanus, but similar to A.mellifera no ortholog of DIF was found. This is in agreement with the recent suggestion that DIF belongs to a highly derived branch possibly found only in brachyceran flies [13]. Therefore, in C. floridanus Dorsal appears to be the unique transcription factor required for induction of AMPs during the Toll mediated immune response.Fig. 5


Scrutinizing the immune defence inventory of Camponotus floridanus applying total transcriptome sequencing.

Gupta SK, Kupper M, Ratzka C, Feldhaar H, Vilcinskas A, Gross R, Dandekar T, Förster F - BMC Genomics (2015)

The Toll signalling pathway of C. floridanus. All identified signalling components are mapped on the comprehensive immune network of D. melanogaster. The names of the factors correspond to the Drosophila designations. Connectivity among nodes is based either on positive attribute (blue arrow) or negative attribute (red arrow). Missing components are shown in grey colour. Nuclear translocation is shown by a green arrow. Factors significantly upregulated on the transcriptional level upon immune-challenge are shown by green boxes
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4508827&req=5

Fig5: The Toll signalling pathway of C. floridanus. All identified signalling components are mapped on the comprehensive immune network of D. melanogaster. The names of the factors correspond to the Drosophila designations. Connectivity among nodes is based either on positive attribute (blue arrow) or negative attribute (red arrow). Missing components are shown in grey colour. Nuclear translocation is shown by a green arrow. Factors significantly upregulated on the transcriptional level upon immune-challenge are shown by green boxes
Mentions: The Toll pathway of insects is mainly activated by fungal pathogens and Gram-positive bacteria. The Toll pathway not only regulates the antimicrobial response but is also required for proper haemocyte proliferation [4, 37]. Therefore, Toll activation leads to a coordinated immune response that comprises both cellular and humoral immunity [38]. The Toll signalling pathway was found to be highly conserved in terms of the presence of homologs in C. floridanus (Fig. 5). Recognition of Lys-type PGN characteristic for most Gram-positive bacteria or of fungal beta-1,3-glucans by specific PRRs leads to the activation of proteolytic cascades which finally activate the Toll-dependent signalling cascade. In C. floridanus three PRRs likely feeding into the Toll pathway are found: a PGRP-SA (Cflo_N_g8526t1) which according to sequence homology probably recognises Lys-type PGN, and two proteins annotated as beta-1,3-glucan binding proteins (Cflo_N_g15215t1 and Cflo_N_g5742t1) with high homologies to both GNBP1 and GNBP3 of D. melanogaster. GNBP1 is known to perceive Lys-type PGN, while GNBP3 recognises fungal cell wall components [39]. The homology data of the C. floridanus proteins do not allow a clear identification of the signal sensed by the two GNBPs. However, the previous expression data acquired post immune challenge of C. floridanus with Gram-negative or Gram-positive bacteria revealed a long-lasting up-regulation of the gene encoding one of the GNBPs (EFN66519.1; Cflo_N_g5742t1) only after infection with Gram-positive bacteria [17]. This suggests that this Camponotus protein may be able to recognise Lys-type PGN and thus may be a functional homolog of GNBP1 of D. melanogaster (Fig. 5). In addition, C. floridanus encodes a homolog of the protease Persephone which was previously shown to be involved in the detection of danger signals indicative for infection with Gram-positive bacteria and fungi [40]. In D. melanogaster the Toll pathway is triggered upon microbially induced proteolytic cleavage of the circulating cytokine-like ligand molecule Spätzle that binds to the Toll receptor, thus finally leading to the nuclear translocation of the NF-κB-like transcription factors Dorsal and DIF (Dorsal-related immunity factor). A single gene encoding Dorsal is present in C. floridanus, but similar to A.mellifera no ortholog of DIF was found. This is in agreement with the recent suggestion that DIF belongs to a highly derived branch possibly found only in brachyceran flies [13]. Therefore, in C. floridanus Dorsal appears to be the unique transcription factor required for induction of AMPs during the Toll mediated immune response.Fig. 5

Bottom Line: Based on homology analysis with key components of major immune pathways of insects, the C. floridanus immune-related genes were compared to those of Drosophila melanogaster, Apis mellifera, and other hymenoptera.The comparison of the immune system of C. floridanus with that of other insects revealed the presence of a broad immune repertoire.However, the relatively low number of PGN recognition proteins and AMPs, the identification of Camponotus specific putative immune genes, and stage specific differences in immune gene regulation reflects Camponotus specific evolution including adaptations to its lifestyle.

View Article: PubMed Central - PubMed

Affiliation: Department of Bioinformatics, Biocentre, University of Würzburg, Am Hubland, D-97074, Würzburg, Germany. shishir.bioinfo@gmail.com.

ABSTRACT

Background: Defence mechanisms of organisms are shaped by their lifestyle, environment and pathogen pressure. Carpenter ants are social insects which live in huge colonies comprising genetically closely related individuals in high densities within nests. This lifestyle potentially facilitates the rapid spread of pathogens between individuals. In concert with their innate immune system, social insects may apply external immune defences to manipulate the microbial community among individuals and within nests. Additionally, carpenter ants carry a mutualistic intracellular and obligate endosymbiotic bacterium, possibly maintained and regulated by the innate immune system. Thus, different selective forces could shape internal immune defences of Camponotus floridanus.

Results: The immune gene repertoire of C. floridanus was investigated by re-evaluating its genome sequence combined with a full transcriptome analysis of immune challenged and control animals using Illumina sequencing. The genome was re-annotated by mapping transcriptome reads and masking repeats. A total of 978 protein sequences were characterised further by annotating functional domains, leading to a change in their original annotation regarding function and domain composition in about 8% of all proteins. Based on homology analysis with key components of major immune pathways of insects, the C. floridanus immune-related genes were compared to those of Drosophila melanogaster, Apis mellifera, and other hymenoptera. This analysis revealed that overall the immune system of carpenter ants comprises many components found in these insects. In addition, several C. floridanus specific genes of yet unknown functions but which are strongly induced after immune challenge were discovered. In contrast to solitary insects like Drosophila or the hymenopteran Nasonia vitripennis, the number of genes encoding pattern recognition receptors specific for bacterial peptidoglycan (PGN) and a variety of known antimicrobial peptide (AMP) genes is lower in C. floridanus. The comparative analysis of gene expression post immune-challenge in different developmental stages of C. floridanus suggests a stronger induction of immune gene expression in larvae in comparison to adults.

Conclusions: The comparison of the immune system of C. floridanus with that of other insects revealed the presence of a broad immune repertoire. However, the relatively low number of PGN recognition proteins and AMPs, the identification of Camponotus specific putative immune genes, and stage specific differences in immune gene regulation reflects Camponotus specific evolution including adaptations to its lifestyle.

No MeSH data available.


Related in: MedlinePlus